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Journal of General Plant Pathology

, Volume 81, Issue 1, pp 32–41 | Cite as

Overexpression of OsHAP2E for a CCAAT-binding factor confers resistance to Cucumber mosaic virus and Rice necrosis mosaic virus

  • Md. Mahfuz Alam
  • Hidemitsu Nakamura
  • Hiroaki Ichikawa
  • Kappei Kobayashi
  • Takashi Yaeno
  • Naoto Yamaoka
  • Masamichi NishiguchiEmail author
Viral and Viroid Diseases

Abstract

HAP (CBF/NF-Y) transcription factors have important functions in regulating plant growth, development, and stress responses. In this study, we examined whether the endogenous gene OsHAP2E and the GUS transgene driven by the promoter of OsHAP2E respond to virus infection. RT-PCR analyses showed OsHAP2E expression was induced after inoculation with Cucumber mosaic virus (CMV) or Rice necrosis mosaic virus (RNMV). After inoculating OsHAP2E::GUS-transgenic plants with either virus, the levels of GUS expression increased significantly. The expression levels of GUS or OsHAP2E reached a plateau 5 days after inoculation of rice with CMV, which paralleled the accumulation of CMV RNA level. Furthermore, transgenically over-expressed lines of OsHAP2E (OsHAP2E-OX) had lower levels of CMV and RNMV RNAs than in in nontransgenic control plants. The OsHAP2E-OX lines developed no significant symptoms from RNMV while control plants had yellowing and stunting. These results suggested that OsHAP2E is induced by virus infection and contributes to resistance against viral pathogens.

Keywords

Cucumber mosaic virus CCAAT GUS Heme activator protein 2E (HAP2E) Rice Rice necrosis mosaic virus 

Notes

Acknowledgments

We thank Drs. C. Masuta and T. Tachibana for the infested soil with P. graminis-carrying RNMV and the use of Retoratome, respectively. We are also grateful to D. Murphy for English editing of the manuscript. This work was supported by the Program for Promotion of Basic and Applied Researches in Bio-oriented Industry, and the Ministry of Education, Culture, Sports, Science and Technology of Japan [Grant-in-Aid for Scientific Research for Scientific Research (C) and (B), No. 24580065 to MN and No. 26292026 to KK] and by grants from the Ministry of Agriculture, Forestry and Fisheries of Japan (Rice Genome Project RMP-2113 to MN; Green Technology Project EF-1001 and EF-1004 to HI).

References

  1. Alam MM, Nakamura H, Ichikawa H, Miyao A, Hirochika H, Kobayashi K, Yamaoka N, Nishiguchi M (2014a) Response of an aspartic protease gene OsAP77 to fungal, bacterial and viral infections in rice. Rice 7:9. doi: 10.1186/s12284-014-0009-2 CrossRefGoogle Scholar
  2. Alam MM, Tanaka T, Nakamura H, Ichikawa H, Kobayashi K, Yaeno T, Yamaoka N, Shimomoto K, Takayama K, Nishina H, Nishiguchi M (2014b) Overespression of a rice heme activator protein gene (OsHAP2E) confers resistance to pathogens, salinity and drought, and increases photosynthesis and tiller number. Plant Biotechnol J. doi: 10.1111/pbi.12239 PubMedGoogle Scholar
  3. Badge JL, Kashiwazaki S, Lock S, Foster GD (1997) A bymovirus PCR primer and partial nucleotide sequence provides further evidence for the recognition of rice necrosis mosaic virus as a bymovirus. Eur J Plant Pathol 103:721–724CrossRefGoogle Scholar
  4. Ballif J, Endo S, Kotani M, MacAdam J, Wu Y (2011) Over-expression of HAP3b enhances primary root elongation in Arabidopsis. Plant Physiol Biochem 49:579–583PubMedCrossRefGoogle Scholar
  5. Chen J, Xia X, Yin W (2009) Expression profiling and functional characterization of a DREB2-type gene from Populus euphratica. Biochem Biophys Res Commun 378:483–487PubMedCrossRefGoogle Scholar
  6. Chen H, Kobayashi K, Yamaoka N, Nishiguchi M (2011) Further analysis of rice RNA-dependent RNA polymerase 1 (OsRDR1) in RNA silencing and antiviral defense. Jpn J Phytopathol 77:59Google Scholar
  7. Dang VD, Bohn C, Bolotin-Fukuhara M, Daignan-Fornier B (1996) The CCAAT box-binding factor stimulates ammonium assimilation in Saccaromyces cerevisiae, defining a mew cross-pathway regulation between nitrogen and carbon metabolisms. J Bacteriol 178:1842–1849PubMedCentralPubMedGoogle Scholar
  8. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371PubMedCrossRefGoogle Scholar
  9. Forsburg SL, Guarente L (1989) Identification and characterization of HAP4: a third component of the CCAAT-bound HAP2/HAP3 heteromer. Genes Dev 3:1166–1178PubMedCrossRefGoogle Scholar
  10. Fujii S (1978) Studies on rice necrosis mosaic virus. Special Bull Okayama Pref Agric Expt Stn 69:81Google Scholar
  11. Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7:465–471PubMedCrossRefGoogle Scholar
  12. Hanada K, Tochihara H (1987) Attenuated CMV. In: Umeya K, Kato H (eds) Microorganisms useful in agriculture: their use and perspectives (in Japanese). Youken-do Press, Tokyo, pp 58–70Google Scholar
  13. Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411PubMedCentralPubMedCrossRefGoogle Scholar
  14. Inouye T, Fujii S (1977) Rice necrosis mosaic virus. CMI/AAB Descr Pl Viruses No. 172Google Scholar
  15. Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405CrossRefGoogle Scholar
  16. Kim MK, Kwak HR, Lee SH, Kim JS, Kim KH, Cha BJ, Choi HS (2011) Characteristics of Cucumber mosaic virus isolated from Zea mays in Korea. Plant Pathol J 27:372–377CrossRefGoogle Scholar
  17. Laloum T, De Mita S, Gamas P, Baudin M, Niebel A (2013) CCAAT-box binding transcription factors in plants: y so many? Trends Plant Sci 18:157–166PubMedCrossRefGoogle Scholar
  18. Lee WK, Seo HY (1992) On eighteen aphids (Tribe aphidini) occurring in Korea with a description of a new species (Homoptera: Aphididae). Korean J Ent 22:101–111Google Scholar
  19. Linhart C, Elkon R, Shiloh Y, Shamir R (2005) Deciphering transcriptional regulatory elements that encode specific cell cycle phasing by comparative genomics analysis. Cell Cycle 4:1788–1797PubMedCrossRefGoogle Scholar
  20. Litzka O, Bergh T, Brakhage AA (1996) The Aspergillus nidulans penicillin biosynthesis gene aat (penDE) is controlled by a CCAAT- containing DNA element. Eur J Biochem 238:675–682PubMedCrossRefGoogle Scholar
  21. Maity SN, de Crombrugghe B (1998) Role of the CCAAT-binding protein CBF/NF-Y in transcription. Trends Biochem Sci 23:174–178PubMedCrossRefGoogle Scholar
  22. Mantovani R (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene 239:15–27PubMedCrossRefGoogle Scholar
  23. Miyoshi K, Ito Y, Serizawa A, Kurata N (2003) OsHAP3 genes regulate chloroplast biogenesis in rice. Plant J 36:532–540PubMedCrossRefGoogle Scholar
  24. Nishiguchi M, Shimono M, Eguchi Y, Okuizumi H, Yazaki J, Nakamura K, Fujii F, Shimbo K, Shimatani Z, Nagata Y, Hashimoto A, Ohta T, Sato Y, Honda S, Iwano M, Yamamoto K, Sakata K, Sasaki T, Kishimoto N, Kikuchi S (2004) Microarray analysis of gene expression in rice treated with probenazole, a resistance inducer, in special reference to blast disease. In: Kawasaki S (ed) Rice blast: interaction with rice and control. Kluwer, Dordrecht, pp 145–154CrossRefGoogle Scholar
  25. Palukaitis P, García-Arenal F (2003) Cucumoviruses. Adv Virus Res 62:241–323PubMedCrossRefGoogle Scholar
  26. Romier C, Cocchiarella F, Mantovani R, Moras D (2003) The NF-YB/NF-YC structure gives insight into DNA binding and transcription regulation by CCAAT factor NF-Y. J Biol Chem 278:1336–1345PubMedCrossRefGoogle Scholar
  27. Shimono M, Yazaki J, Nakamura K, Kishimoto N, Kikuchi S, Iwano M, Yamamoto K, Sakata K, Sasaki T, Nishiguchi M (2003) cDNA microarray analysis of gene expression in rice plants treated with probenazole, a chemical inducer of disease resistance. J Gen Plant Phathol 69:76–82CrossRefGoogle Scholar
  28. Shohara K, Osaki T (1974) Precipitation and purification of Cucumber mosaic virus by polyethylene glycol (PEG) and reverse concentration PEG gradient centrifugation. Ann Phytopath Soc Japan 40:265–267CrossRefGoogle Scholar
  29. Stephenson TJ, McIntyre CL, Collet C, Xue GP (2010) TaNF-YC11, one of the light-upregulated NF-YC members in Triticum aestivum, is co-regulated with photosynthesis-related genes. Funct Integr Genomics 10:265–276PubMedCrossRefGoogle Scholar
  30. Thirumurugan T, Ito Y, Kubo T, Serizawa A, Kurata N (2008) Identification, characterization and interaction of HAP family genes in rice. Mol Genet Genomics 279:279–289PubMedCrossRefGoogle Scholar
  31. Thomas MC, Chiang CM (2006) The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 41:105–178PubMedCrossRefGoogle Scholar
  32. Usugi T, Saito Y (1976) Purification and serological properties of barley yellow mosaic virus and wheat yellow mosaic virus (in Japanese with English summary). Ann Phytopath Soc Japan 42:12–20CrossRefGoogle Scholar
  33. Usugi T, Kashiwazaki S, Omura T, Tsuchizaki T (1989) Some properties of nucleic acids and coat proteins of soil-borne filamentous viruses. Ann Phytopath Soc Japan 55:26–31CrossRefGoogle Scholar
  34. van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162PubMedCrossRefGoogle Scholar
  35. Wei X, Xu J, Guo H, Jiang L, Chen S, Yu C, Zhou Z, Hu P, Zhai H, Wan J (2010) DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol 153:1747–1758PubMedCentralPubMedCrossRefGoogle Scholar
  36. Zenbayashi R, Hanada K, Tochihara H (1987) Control of tomato mosaic disease by spray inoculation of attenuated strains of cucumber mosaic virus (in Japanese). Annu Rep Kanto-Tosan Plant Prot Soc 34:50–51Google Scholar
  37. Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10:29PubMedCentralPubMedCrossRefGoogle Scholar
  38. Zhou GH, Chen JB, Chen SM (1990) Comparative identification of wheat spindle streak mosaic virus from different plants in China (in Chinese with English summary). Acta Phytopathol Sin 20:107–110Google Scholar

Copyright information

© The Phytopathological Society of Japan and Springer Japan 2014

Authors and Affiliations

  • Md. Mahfuz Alam
    • 1
  • Hidemitsu Nakamura
    • 3
    • 4
  • Hiroaki Ichikawa
    • 3
  • Kappei Kobayashi
    • 1
    • 2
  • Takashi Yaeno
    • 1
    • 2
  • Naoto Yamaoka
    • 1
    • 2
  • Masamichi Nishiguchi
    • 1
    • 2
    Email author
  1. 1.The United Graduate School of Agricultural SciencesEhime UniversityMatsuyamaJapan
  2. 2.Faculty of AgricultureEhime UniversityMatsuyamaJapan
  3. 3.National Institute of Agrobiological SciencesTsukubaJapan
  4. 4.Department of Applied Biological Chemistry, Graduate School of Agricultural Life SciencesThe University of TokyoTokyoJapan

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